Full text of DOI:10.1359/jbmr.2001.16.1.141

JOURNAL OF BONE AND MINERAL RESEARCH
Volume 16, Number 1, 2001
© 2001 American Society for Bone and Mineral Research
Bone Mineral Changes in Obese Women During a
Moderate Weight Loss With and Without Calcium
Supplementation
LARS BJØRN JENSEN,1 GINA KOLLERUP,1 FLEMMING QUAADE,2 and OLE HELMER SØRENSEN1
ABSTRACT
A significant relationship between body weight (BW) and bone mass (BM) has been established previously. A
diet-induced weight loss is accompanied by a significant decrease in bone mineral density (BMD) and total
body bone mineral (TBBM), but the underlying mechanisms are not clarified. Sixty-two obese women were
included in the study. Dual-energy X-ray absorptiometry (DXA) and measurements of a series of calcium-
regulating hormones and biochemical markers of bone turnover were performed at baseline and after 1 month
and 3 months on a low calorie diet. Thirty of the women were randomized to a daily supplement of 1 g of
calcium. After an additional 3 months without dietary prescriptions or calcium supplements, a subgroup of 48
subjects (24 from each group) were scanned again using DXA. There was a significant decrease in TBBM after
1 month and 3 months. A similar pattern was observed in the bone mineral content (BMC) of the lumbar spine
in the patients who did not receive a calcium supplement, whereas no changes occurred in the supplemented
group. The initial calcium supplementation seemed to protect against bone loss in the lumbar spine but not in
the TBBM. In the nonsupplemented group, a statistically significant inverse correlation was found between the
calcium/creatinine ratio in the morning urine and the changes in BMC of the lumbar spine. Such a
relationship was not seen in the calcium-supplemented group. In the nonsupplemented group, no significant
biochemical changes were observed, whereas a significant decrease in serum parathyroid hormone (PTH) was
seen in the calcium-supplemented group. This might explain some of the protective effects of calcium
supplementation on trabecular bone mass. We conclude that a diet-induced weight loss is accompanied by a
generalized bone loss, which probably is explained mainly by a reduced mechanical strain on the skeleton. This
loss can be partly inhibited by a high calcium intake. Therefore, a calcium supplementation should be
recommended during weight loss, even if the diet contains the officially recommended amounts of calcium.
(J Bone Miner Res 2001;16:141–147)
Key words: weight loss, bone mineral loss, low calorie diet, calcium supplement, formula diet
correlation of BM to BW indicates that a readjustment of
BM must take place subsequently to alterations in BW.
The three body components—TBBM, FM, and lean body
mass (LBM)—can be measured separately by dual-energy
INTRODUCTION
SIGNIFICANT relationship between body weight (BW)
and bone mass (BM) and between total body bone
A
mineral (TBBM) and body fat mass (FM) has been estab- X-ray absorptiometry (DXA), a method whereby the bone
lished in pre- and postmenopausal women.(1–3) The positive mineral measurements, only in extreme situations, are in-
1Osteoporosis Research Center, Hovedstadens Sygehusfællesskab Hvidovre Hospital, Copenhagen, Denmark.
2The Obesity Clinic, Moltkesvej, Copenhagen, Denmark.
141

142
JENSEN ET AL.
fluenced by changes in adjacent fat tissue, and therefore it is personal reasons. Of the remaining 52 women, 14 were
convenient for monitoring the skeleton in subjects who are postmenopausal and 8 of these were in the no-treatment
losing weight.(4–8) Both regional bone mineral and TBBM group.
can be evaluated with high precision and accuracy.(4,9,10)
Whole body measurements of the bone mineral content
A diet-induced weight loss is accompanied by a signifi- (BMC), FM, and fat free mass (FFM) (CV 1.1, 1.6, and
cant decrease in bone mineral density (BMD) and 1.6%, respectively (8,17)) and regional measurements of
TBBM,(8,11) and one study indicates that a 1 g/day calcium the lumbar and femoral BMC (CV 1% and 1.5% respec-
substitution can suppress bone turnover in energy-restricted tively(18)) were performed by a Hologic QDR-2000 DXA
subjects.(12) The underlying mechanisms for the bone scanner (Hologic Inc., Westham, MA, USA) using the
changes are not clear. Suggested explanations are: (1) pencil-beam mode, at baseline after 1 month and after 3
weight relief on the bones causes an adjustment of the months in 52 women. Twenty-four women (6 postmeno-
skeleton probably mediated by humoral factors; (2) second- pausal) from each group were rescanned 6 months from
ary hyperparathyroidism has been described in obese pa- baseline. To obtain the best possible comparability at
tients but, during weight loss, an increase in Ca2ϩ is seen follow-ups, the baseline regional scans were restored in the
followed by a decrease in parathyroid hormone (PTH),(13,14) scanner and the compare facility was applied, so that cor-
which causes increased renal calcium loss as a result of responding areas were analyzed at baseline and follow-ups.
increased ultrafiltration and decreased reabsorption of cal- Fasting blood samples were drawn in the morning. Serum
cium; (3) diminished extraovarial estrogen synthesis; and was stored at Ϫ20°C. All samples were analyzed in dupli-
(4) though the calcium supplied by weight-reducing diets cate in the same assays. Urine was collected as the second
generally may have been sufficient by current recommen- void fasting morning urine. Serum concentrations of osteo-
dations, obese patients losing weight may have a higher calcin were measured by a bovine ELISA assay (DAKO,
calcium demand, either because of the increased loss of Glostrup, Denmark), and serum 25-hydroxyvitamin D
calcium mentioned previously or because of reduced intes- [25(OH)D] and 1,25-dihydroxyvitamin D [1,25(OH)2D]
tinal absorption.
were measured by competitive protein binding assays using
The purpose of the present investigation was: (1) to rachitic rat kidney cytosol and thymus receptor, respec-
measure changes in the skeleton in relation to changes in the tively. Intact serum PTH was measured by an immunora-
body composition in obese patients undergoing a moderate diometric assay (Allegro Intact PTH; Nichols Institute, Ni-
weight loss on a low calorie regimen; (2) to relate a number chols Institute Diagnostics, Los Angeles, CA, U.S.A.).
of biochemical markers of bone metabolism and calcium Urinary calcium and creatinine were analyzed by standard
regulating hormones to the changes in the BM; and (3) to methods and pyridinoline and urine-deoxypyridinoline were
investigate the influence of a calcium supplement on bone analyzed by high-performance liquid chromatography and
loss in obese persons during a low calorie diet.
fluorescence detection after hydrolysis of the urine as pre-
viously described.(19)
The study fulfilled the Helsinki declaration and was ap-
proved by the local ethics committee. All participants gave
informed consent to participate in the study.
MATERIALS AND METHODS
Sixty-two obese women (body mass index [BMI], 25.2–
51.6 kg/m2) with a motivation for weight loss were included
in the study and randomized at baseline to no treatment or
to 1 g (26 mmol) of calcium supplement (Calcium-Sandoz;
Sandoz, Tietgensgade, Copenhagen, Denmark) in the first 3
months.(12,15) The result of the randomization was open and
no placebo was used. All women attended an outpatient
clinic and underwent initial physical examination and his-
tory. Seventeen of the women were postmenopausal. Eight
of these were in the treatment group. Estrogen substitution
was an exclusion criterion as well as severe somatic dis-
eases and metabolic calcium disturbances.
A formula diet (NUPO; Oluf Mørk Ltd., Glostrup, Den-
mark) yielding 1.9 MJ with a qualitatively free supplement
of food and drink up to 4.2 MJ(16) was prescribed for the
first 3 months. The daily amount of formula diet contained
58 g of protein, 800 mg of calcium, 800 mg of phosphate,
and 200 IU of vitamin D. After the first 3 months the
patients continued on a normal diet but were advised to
reduce the calorie intake.
Statistical analysis
The multivariate analysis of variance (MANOVA) re-
peated measures design, Tukey’s post hoc test, Student’s
t-tests, and Pearson’s linear regression analysis were used
where appropriate. Statistically significant changes over
time are marked with an asterisk at the end of the tables.
Statistically significant differences between groups are
marked with an asterisk in the right margins, except in cases
in which the precise p values are tabulated. When statisti-
cally significant bone changes were found, correlations of
these to weight changes and to bone markers in blood and
urine were calculated. The values of p Ͻ 0.05 were consid-
ered statistically significant. The statistical package “Systat
for the Macintosh” (Systat, Inc., Evanston, IL, U.S.A.) was
used for all statistical analysis.
RESULTS
BW
Of the initial 62 women, 4 women were excluded from
the study during the first month because of lack of compli-
The differences between groups were not statistically
ance and no weight loss, 2 women failed to take the pre- significant at baseline. The mean weight losses in the first
scribed calcium supplement, and 4 women left the study for month were 3.3 kg and 3.1 kg in the untreated group and in

BONE MINERAL CHANGES IN OBESE WOMEN
143
the calcium-supplemented group, respectively. The corre-
sponding weight losses in the following 2 months were 2.9
kg and 2.3 kg. At the 6-month follow-up the untreated group
had regained 1.4 kg while the calcium-supplemented group
had no overall weight change. The changes in BMI followed
the same pattern (Table 1).
BMC
The differences between groups were not statistically
significant at baseline. The mean changes in the BMC of the
lumbar spine, right hip, and whole body are shown in Table
1. There were no mean bone changes in the first month in
the lumbar spine or in the hip, but the untreated patients lost
on average 1.5% of TBBM, and the supplemented group
lost 2.0% of TBBM in that period. There were significant
bone losses (2.0% and 2.2%) in the lumbar spine after 3
months and 6 months in the untreated group but not in the
supplemented group. The unadjusted difference between
groups was borderline statistically significant (p ϭ 0.055),
but adjustment for the initial weight loss decreased the value
of p Ͻ 0.01.
The same tendency was found in the right hip with a
4.0%, though not statistically significant, bone loss after 6
months in the untreated group only.
The decline in TBBM was statistically significant already
after 1 month in both groups (Table 1).
Weight-loss and BMC in the lumbar spine
The relationships between the changes in the BMC in the
lumbar spine and the weight losses after 1, 3, and 6 months
are shown in Table 2. The change in BMC in the lumbar
spine after 6 months was significantly correlated to the
weight changes after 1 month and 3 months but not to the
weight change after 6 months and only in the untreated
group. The weight loss after 1 month did not correlate to the
BMC change after 1 month but accounted for 25% of the
variation in the BMC change after 6 months.
Biochemical parameters
The serum levels of osteocalcin, 25(OH)D and
1,25(OH)2D, and PTH are shown in Table 3. There was an
overall tendency to an increase in the osteocalcin, especially
in the first months and especially in the untreated group. The
increase was statistically significant after 1 month in the
untreated group. No significant changes occurred in
25(OH)D and 1,25(OH)2D. The PTH declined in the treated
group with 11.5% after 1 month, 15.5% after 3 months, and
19.6% after 6 months (p Ͻ 0.05%, p Ͻ 0.01%, and p Ͻ
0.05%, respectively). The changes in PTH and the bone
changes did not correlate.
The calcium/creatinine ratio and the concentrations of
pyridinoline and deoxypyridinoline in the spot urine are
shown in Table 4.
The calcium/creatinine ratio increased after 1 month and
remained significantly elevated after 3 months in the treated
group. In the untreated group the 3-month value showed an

144
JENSEN ET AL.
TABLE 2. CHANGES IN THE BMC IN THE LUMBAR SPINE RELATED TO CHANGES IN THE BW
Bone change after 1 month
Without calcium (n ϭ 27)
With calcium (n ϭ 25)
␤-Estimates (g/kg)
p Values
0.95
␤-Estimates (g/kg)
Ϫ0.40
p Values
0.14
Differences
p Values
Weight changes in 1 month
0.02
0.62
NS
Bone change after 3 months
Without calcium (n ϭ 27)
With calcium (n ϭ 25)
␤-Estimates (g/kg)
p Values
␤-Estimates (g/kg)
p Values
Differences
p Values
Weight changes in 1 month
Weight changes in 3 months
0.68
0.20
0.08
0.22
Ϫ0.09
Ϫ0.05
0.72
0.62
0.77
0.25
NS
NS
Bone change after 6 months
Without calcium (n ϭ 24)
With calcium (n ϭ 24)
␤-Estimates (g/kg)
p Values
␤-Estimates (g/kg)
p Values
Differences
p Values
Weight changes in 1 month
Weight changes in 3 months
Weight changes in 6 months
1.29
0.47
0.19
0.01
0.02
0.11
0.09
0.01
0.00
0.73
0.96
0.98
1.20
0.46
0.19
Ͻ 0.01
Ͻ 0.05
NS
The ␤-estimates are the Pearson regression coefficients from the correlations between the changes in the BW and the changes in the BMC.
TABLE 3. OSTEOCALCIN AND CALCIOTROPIC HORMONES IN SERUM
Osteocalcin (␮g/liter)
25(OH)D (ng/ml)
Calcium
1,25(OH)2D (pg/ml)
Calcium
PTH (pmol/liter)
Calcium
Calcium
Untreated supplement Untreated supplement Untreated supplement Untreated supplement
n
24 25 24 25 24 25 22 25
Baseline
1 Month
7.51 (0.34) 6.83 (0.22) 16.2 (1.5) 21.7 (3.0) 29.5 (2.2) 28.2 (2.5) 3.44 (0.31) 4.01 (0.34)
7.84 (0.32) 6.98 (0.22) 4.34 (0.73) 3.55 (0.21)
7.92 (0.25) 6.91 (0.19) 17.5 (1.5) 18.8 (1.8) 27.8 (2.2) 26.4 (1.4) 3.70 (0.60) 3.39 (0.22)
—
—
—
—
3 Months
6 Monthsa
7.80 (0.30) 7.02 (0.22)
—
—
—
—
3.47 (0.36) 3.35 (0.32)
Changes from baseline
After 1 month
After 3 months
After 6 monthsa
4.4%*
5.5%
2.6%
2.2%
1.2%
3.5%
—
8.0%
—
—
Ϫ13.4%
—
—
Ϫ5.8%
—
—
Ϫ6.4%
—
26.2%
7.6%
0.7%
Ϫ11.5%*
Ϫ15.5%†
Ϫ19.6%*
The means and SEMs at baseline and after 1, 3, and 6 months are shown.
a n ϭ 22 in each group at the 6-month follow-up.
* p Ͻ 0.05; † p Ͻ 0.01.
increasing tendency. Urinary pyridinoline and deoxypyr-
idinoline did not change.
DISCUSSION
In agreement with earlier investigations,(8,11) a close cor-
relation was observed in the present study between weight
loss and TBBM loss. We found similar changes in the
lumbar spine and in the proximal femur regions that are
Changes in the calcium/creatinine ratio in spot urine
and the BMC in the lumbar vertebrae
The relationships between the changes in the BMC in the especially exposed to osteoporotic fractures. No mineral
lumbar spine and the changes in urine calcium/creatinine was lost in the lumbar spine when a 1 g calcium supplement
ratios after 1 month and 3 months are shown in Table 5.
was prescribed, in addition to the formula diet already
There was a uniform pattern with a negative correlation yielding sufficient calcium. This is a new observation that
between the changes in the urine calcium/creatinine ra- might have practical implications for future treatment of
tios and the changes in the lumbar BMC in the untreated obesity and may suggest some explanation for the bone
group.
changes accompanying weight loss.

BONE MINERAL CHANGES IN OBESE WOMEN
145
TABLE 4. URINARY CALCIUM AND PYRIDINOLINES
Calcium/creatinine ratio
Calcium
Pyridinoline
Calcium
Deoxypyridinoline
Calcium
Untreated
supplement
Untreated
supplement
Untreated
supplement
n
26
25
26
25
26
25
Baseline
1 Month
3 Months
0.41 (0.06)
0.41 (0.07)
0.50 (0.09)
0.24 (0.03)*
0.33 (0.04)
0.32 (0.04)
54.1 (4.0)
56.0 (3.9)
55.3 (3.1)
43.3 (2.5)*
43.5 (2.3)
47.9 (3.1)
16.4 (1.4)
17.0 (1.3)
16.3 (0.9)
12.8 (0.9)*
12.3 (0.8)
13.2 (0.9)
Changes from baseline
After 1 month
After 3 months
0.0%
22.0%
37.5%
33.3%*
3.5%
2.2%
0.5%
10.6%
3.7%
Ϫ0.6%
Ϫ3.9%
3.1%
* p Ͻ 0.05.
The means and SEMs at baseline and after 1 month and 3 months are shown.
TABLE 5. CHANGES IN THE BMC IN THE LUMBAR SPINE RELATED TO CHANGES IN THE URINE CALCIUM/CREATININE RATIO
Bone changes after 1 month
With calcium
Without calcium
␤-Estimate p Value
Ϫ1.571
␤-Estimate (g)
p Value
Difference
p Value
Calcium/creatinin ratio changes in 1 month
1.600
0.43
0.04
3.171
NS
Bone changes after 3 months
Calcium/creatinin ratio changes in 1 month
Calcium/creatinin ratio changes in 3 months
0.744
3.268
0.69
0.24
Ϫ0.965
Ϫ0.267
0.37
0.21
1.709
3.535
NS
NS
Bone changes after 6 months
Calcium/creatinin ratio changes in 1 months
Calcium/creatinin ratio changes in 3 months
1.963
4.197
0.33
0.18
Ϫ2.549
Ϫ2.246
0.09
0.08
4.512
6.443
NS
0.05
The ␤-estimates are the Pearson regression coefficients from the correlations between changes in the calcium/creatinine ratios and the
changes in the BMC.
The urinary calcium excretion analyses confirm the bone integrins, which are receptors through which cells attach the
changes and to some degree the theory of impaired calcium matrix where the strain is produced.(23) Local effects might
supply. When no calcium supplement was given, urinary be mediated through prostaglandins, cytokines, and growth
calcium and BMC changes in the lumbar spine were corre- factors.
lated in the expected manner, with increasing loss of cal-
The hormone leptin, which seems to have a central ap-
cium in the urine accompanying loss of BMC. PTH de- petite regulating action, is greatly influenced by weight loss
creased in the calcium-supplemented group, an expected and recently has been investigated in the light of bone
effect of calcium supplementation. Suppression of PTH will metabolism.(24–27) We did not measure serum leptin in our
result in a reduced bone resorption and thus a reduced loss patients, but other studies point in the direction that covaria-
of bone.
tion between bone mass and leptin is caused by the strong
The changes in bone mass probably are induced by local correlation between leptin and BW and between BW and
factors and by changes in the mechanostat described by bone mass, and that leptin has only marginal, if any, direct
Frost.(20) According to Frost, the mechanostat comprises effect on the bone mass in the mature skeleton.(26,27) The
one or more mechanisms that orchestrate the biological situation seems to be more complex if the skeleton is still
activities that maintain the skeleton’s architecture and growing, and correlation analyses suggest a positive effect
strength. It is not known which cells participate in the of leptin on BMD in children.(25)
regulation, but according to Frost et al.(21) it is neither the
The present study includes measurements after 1 month
osteoblasts nor the osteoclasts. In recent years there has and at the end of the diet. Therefore, it is possible to
been increasing experimental support that the osteocytes, evaluate the timing of the bone changes in relation to the
through their extensive network, are able to detect changes weight changes. Although half of the weight loss took place
in bone strain and thereby to control bone modeling and in the first month, it took 3 months before there was any
remodeling.(22) The molecular mechanisms by which the detectable bone loss in the lumbar spine, and the lumbar
cells perceive changes in mechanical loading are not exactly bone status was much better predicted from the weight
known, but one attracting theory is the involvement of status after 1 month than from the weight status after 6

146
JENSEN ET AL.
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The most convincing effect of the calcium substitution
was in the lumbar spine. The loss of TBBM on the other
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found significant losses in TBBM and lumbar BMC in the
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26. Odabasi E, Ozata M, Turan M, Binga`l N, Ya`nem A, Cakir B, Received in original form December 17, 1999; in revised form
Kutlu M, Ozdemir IC 2000 Plasma leptin concentrations in May 25, 2000; accepted July 24, 2000.